Intraspecific variation in limblessness in vertebrates: a unique example of microevolution

Many species of arboreal marine snails in the genus Littoraria are polymorphic for shell colour, with morphs that correspond in both colour and frequency to those predominant in the habitat. Although the combined effects of selection for crypsis and apostasy have been suggested as the most likely reasons for this, they have not been demonstrated directly in the field. We investigated whether two parasitoid flies, Sarcophaga megafilosia and Sarcophaga meiofilosia, select for crypsis in Littoraria filosa . It was possible to compare the proportions that matched and did not match the background between samples of live and dead snails because the shells of individuals killed by these parasitoids, within which the larva and pupa develop, remain attached to the substratum. This comparison was necessary because these snails frequently move among different coloured microhabitats, which will tend to obscure any effect of selection for crypsis if only live individuals are censused. The method appeared reliable since there was no change in background colour and very little loss of shells between larviposition and emergence of flies. S. megafilosia killed a significantly greater than expected proportion of snails that did not match their background. In contrast, there was no evidence of selective attack by S. meiofilosia. These results are discussed in relation to previous work on polymorphisms in Littoraria species. We also suggest that the role of parasitoid insects as selective agents contributing to the maintenance of colour polymorphisms in terrestrial molluscs may have been overlooked.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77, 367−377.     

Epistasis, phenotypic disequilibrium and contrasting associations with climate in the land snail Theba pisana

Hotter conditions favour effectively unbanded (EUB) shells in the snail Theba pisana. T. pisana is also polymorphic for colour of the shell's apex, determined by a pair of alleles at a locus linked to the banding locus. Apex colour is epistatic to shell banding, such that banded snails with a dark apex have darker bands. Annual censuses over 22 years across an ecotone between a sheltered Acacia thicket and open dune vegetation showed a persistent association of both EUB shells and pale apex with the Open habitat. The parallel variation was due partly to strong phenotypic disequilibrium, as the combination of EUB with dark apex was rare. Nevertheless, in fully banded shells the frequency of pale apex was also higher in the Open habitat, confirming independent, parallel associations of the two contributors to paleness. Within the Acacia habitat, temporal variation of the frequencies of banding morphs was much greater than for apex colour, and EUB shells were associated with hotter summers. Consistent with its primary effect only on the very small snails, apex colour did not vary with summer conditions, but instead, higher frequencies of pale apices were associated with sunnier winters. The intensity of selection was lower on apex colour than shell banding, due partly to the constraint of phenotypic disequilibrium. The shell traits in T. pisana are an example of complex responses to climatic variation, in which phenotypic disequilibrium constrains evolution of apex colour, but separate mechanisms of selection are evident.     

Apostasy and selection for crypsis in the marine snail Littoraria filosa: an explanation for a balanced colour polymorphism

The marine snail, Littoraria filosa, is polymorphic for shell colour, with yellow, brown, and pink morphs that correspond in both appearance and frequency to the predominant background colours of its habitat. Previous research on this polymorphism has found indirect evidence of apostatic selection and selection for crypsis by unknown agents, probably crabs, and direct evidence of selection for crypsis by the parasitoid fly Sarcophaga megafilosia. In the present study, we report on field experiments to investigate whether S. megafilosia and shell‐crushing predators exert apostatic selection on L. filosa. For S. megafilosia, seven experimental treatments containing yellow and brown snails in the proportions of 0.1, 0.2, 0.4, 0.5, 0.6, 0.8, and 0.9 of each colour were established on mangrove trees and used to separately quantify the proportions of each colour attacked on grey/brown trunks and yellow/green leaves. The results obtained confirmed an earlier finding of selection for crypsis, but only showed slight, but significant, anti‐apostatic selection by S. megafilosia. For shell‐crushing predators, seven experimental treatments containing yellow and brown snails in the proportions of 0.08, 0.17, 0.33, 0.50, 0.66, 0.83, and 0.92 were established on two types of trees that differed in their background proportions of brown and green: (1) trees which had been pruned of approximately 90% of their foliage and (2) unpruned trees. The results obtained showed both selection for crypsis and apostatic selection. Furthermore, a selectively neutral frequency for yellow L. filosa was found for each background, and was less on pruned trees than unpruned ones (and vice versa for brown L. filosa), which can therefore account for the maintenance of a colour polymorphism where the proportions of each morph tend to resemble and correspond in frequency to the colours of the background. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 62–71.     

Differences in predatory pressure on terrestrial snails by birds and mammals

The evolution of shell polymorphism in terrestrial snails is a classic textbook example of the effect of natural selection in which avian and mammalian predation represents an important selective force on gene frequency. However, many questions about predation remain unclear, especially in the case of mammals. We collected 2000 specimens from eight terrestrial gastropod species to investigate the predation pressure exerted by birds and mice on snails. We found evidence of avian and mammalian predation in 26.5% and 36.8% of the shells. Both birds and mammals were selective with respect to snail species, size and morphs. Birds preferred the brown-lipped banded snail Cepaea nemoralis (L.) and mice preferred the burgundy snail Helix pomatia L. Mice avoided pink mid-banded C. nemoralis and preferred brown mid-banded morphs, which were neglected by birds. In contrast to mice, birds chose larger individuals. Significant differences in their predatory pressure can influence the evolution and maintenance of shell size and polymorphism of shell colouration in snails.     

Gene regulation of shell banding in a land snail from Israel

The Israeli land snail, Xeropicta vestalis, offers a particularly clear example of gene regulation in relation to natural selection, in that within each population the appropriate phenotype is generated only at the correct part of the animals life cycle, and a contrasting phenotype develops when the forces of natural selection change. In the mountains of Jerusalem, where the winter is cold, the shells are dark. Westwards, towards the coastal plain where the winter is warmer, the shells gradually become paler. As dark shells absorb more radiation than pale ones, this clinal variation in morph frequencies can be explained in thermal terms. (Banded shells are also more cryptic than non-banded shells, so that in the mountains visual selection by predators may be an additional force which favours dark shells.) Xeropicta vestalis is an annual, semelparous species: the snails hatch in winter, become mature within one year, reproduce, and then die. In the coastal plain the snails are active throughout most of the year, and they have a long period in which to grow to reach adult size. In the mountains and hills, on the other hand, the snails are active for only a very short period. They spend most of their lives as small snails, in a state of aestivation. Xeropicta vestalis must be dark in mountains because when it finally awakens, it must very rapidly and hastily reach reproduction size. A dark shell, by speeding up temperature-dependent processes in this critical stage, assists the snail to mature rapidly. Shell darkness varies with age: in the mountains and hills the shells are moderately dark when they hatch, but become darker whilst growing in early winter. In the coastal plain also, the snails are moderately dark when they hatch; but here they become paler, whilst growing in winter and spring. In both cases, each snail is darker in the colder months and paler in the hot ones. A strategy of gene regulation of shell colour is thus favoured when the subsequent forces of the environment are very contrasting in their direction, very severe—yet also very predictable.     

Selective predation favouring cryptic individuals of marine snails (Littorina)

Many gastropods have inherited conspicuous shell colour polymorphisms. A challenging question is, are colour frequencies under selection or is polymorphism owing to random evolutionary processes? The intertidal species Littorina saxatilis (a rock‐dweller) and L. obtusata (confined to macroalgae) both have genetically determined shell colour variation. In Iceland, Littorina obtusata are mostly cryptic on brown macroalgae by having brown or yellow shells (~95% of the snails), while Littorina saxatilis often appears conspicuous to the background of dark rocks owing to non‐cryptic colours (15–20%). This difference may be due to selective elimination of conspicuously coloured L. obtusata by visual predators, while L. saxatilis, largely living in another habitat, is not under a similarly intense colour selection. To test this hypothesis we increased the frequencies of conspicuous L. saxatilis in experimental populations (from <12 to 55%) and placed these in the seaweed zone, the main habitat of L. obtusata. Fifteen populations were released on isolated spots of seaweed and three of these were covered by net cages to exclude bird predators. One month later, yellow snails had increased in frequency within the patches, and to our surprise the result did not differ between bare and caged patches. This suggests selection favouring a colour that matches the background of fucoid seaweeds by visual predators able to enter the cages. Birds acted as important predators by picking 16% of the experimental snails in the uncaged spots, but were unable to enter the caged spots. However, the bird predation was non‐selective with respect to snail colour. For various reasons the most likely predators able to enter the cages were intertidal fish, these were thus responsible for the selection of non‐cryptic snails. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76 , 137–144.     

QUANTITATIVE GENETICS OF SHELL FORM OF AN INTERTIDAL SNAIL: CONSTRAINTS ON SHORT-TERM RESPONSE TO SELECTION

We investigated the genetic and environmental determinants of shell form in an intertidal snail (Prosobranchia: Littorina sp.) to identify constraints on the short-term response to selection. Our quantitative genetic parameters were estimated from a half-sib experimental design using 288 broods of snails. Each brood was divided into two treatments differing in snail population density, and therefore in grazing area per snail. Differences in population density induced marked differences in shell form. Snails in the low density treatment grew faster and had lighter shells with narrower whorls and narrower apertures than their siblings at high density. Despite this environmental plasticity in shell shape we found significant additive genetic variance for components of shell shape. We discuss two mechanisms that may maintain additive genetic variance for shell shape in intertidal snail populations: migration between environments with different selective pressures and migration between environments with different mean growth rates. We also estimated a genetic variance-covariance matrix for shell form traits and used the matrix to identify constraints on the short-term response to selection. We predict the rate of response to selection for predator-resistant morphology such as would occur upon invasion of predatory crabs. The large negative genetic correlation between relative spire height and shell weight would facilitate simultaneous selection for a lower spire and a heavier shell, both of which would increase resistance to predatory crabs.     

Invasion dynamics of the snail Pseudoplotia scabra in Lake Kinneret

The freshwater snail Pseudoplotia scabra Müller (Thiaridae) was first spotted in Lake Kinneret, Israel, in the mid 2000s. In a series of field surveys we followed its spread, documenting how by the end of 2010 this invasive mollusc formed >95 % of the snails in Lake Kinneret, nearly eradicating four native species.     

The effect of calcium and pH on Florida apple snail, Pomacea paludosa (Gastropoda: Ampullariidae), shell growth and crush weight

Pomacea (Ampullariidae) snails, commonly referred to as apple snails, serve as prey for many freshwater-dependent predators, and some species are highly invasive. Identifying limits to apple snail distribution and abundance are pertinent to understanding their ecology. Calcium (Ca²⁺) availability and pH generally influences freshwater snail populations, yet scant data exist for Pomacea snails. We measured 6-week change in shell length (ΔSL) in P. paludosa in two laboratory experiments with varying Ca²⁺ and pH levels. ΔSL was significantly higher in ≥28 mg Ca²⁺/l compared with treatments ≤14 mg/l. Snails from populations living in low Ca²⁺/pH waters did not appear genetically predisposed at growing faster in these conditions. Smallest ΔSL was in snails treated with 3.6 mg Ca²⁺/l and pH < 6.5 water; these snails had signs of shell erosion. Shell crush weights (CWs) were lowest for snails grown in the lowest Ca²⁺/pH treatment. Smaller shells and lower CWs have implications for predation vulnerability and reproductive success. Our results are consistent with reports associating relatively low snail densities with relatively low Ca²⁺/pH waters, and they are consistent with the geographic distribution of P. paludosa as related to the underlying water chemistry as influenced by geology.     

The effect of experience on the selective behaviour of song thrushes feeding on artificial populations ofCepaea (held)

Song thrushes fed on populations of bread-stuffedCepaea shells. The results indicate that experience influences the selective behaviour of thrushes for both shell colour and shell size. Such behaviour could lead to frequency dependent selection in natural populations. Within the ranges of size and colour offered, thrushes learned from a colour rather than a size experience when both were varied simultaneously.     

Prey preferences in captivity of the freshwater crab Potamonautes lirrangensis from Lake Malawi with special emphasis on molluscivory

Freshwater crabs play an important role for the diversification of shell morphologies in freshwater gastropods. For example, the radiation of the freshwater crab genus Platythelphusa in Lake Tanganyika is thought to have driven shell diversification of the lake’s snail fauna, promoting the evolution of thalassoid shells. No comparable thalassoid snails are known from Lake Malawi. Accordingly, it was hypothesized that the lake’s only freshwater crab, Potamonautes lirrangensis, is not a snail predator. We tested this hypothesis using feeding experiments with specimens caught in the southern part of Lake Malawi. Individual crabs were held in experimental containers offshore and were presented with various food items overnight, after which ingestion frequency was recorded. Potamonautes lirrangensis can be characterized as a scavenger that is opportunistically carnivorous. A preference for fish and snail flesh could be observed, indicating a bias toward carnivory. We observed occasional cracking of the shell in different snail species, with frequent ingestion of artificially crushed specimens, suggesting that crabs do attempt to feed on snails. However, the investigated Lake Malawi gastropods appear to be partly protected against crab predation through thick-walled and low-spired shells (especially Lanistes and Bellamya), obviating the evolution of thalassoid shells carrying rims, ridges, or spines.     

Shell-banding polymorphism of the land snail Xeropicta vestalis along the coastal plain of Israel

Along the coastal plain of Israel, shell darkness of the polymorphic land snail Xeropicta vestalis is positively related to the extent of perennial vegetation. It is not related to rain, temperature, geographic position or darkness of the ground.
White shells reflect more radiation than dark ones do, and therefore in Israel's coastal plain, where solar radiation is very strong, they are favoured. Perennial vegetation, where it occurs, shields the snails from the sun by absorbing radiation, so that snails amongst them can afford to be darker, and thus more cryptic. Hence, the more perennial vegetation in the habitat, the darker the shells.
Also during the Pleistocene, when temperatures were 5–10°C lower than today, the shells of the coastal plain were as pale as recent ones are. The distribution of a snail-predator, Gerbillus allenbyi , which is restricted to sandy biotopes where perennial bushes occur, and which was absent from Israel during the Pleistocene, could perhaps explain the distribution of X. vestalis morphs, both today and in the past.     

Effects of trematode parasitism on the shell morphology of snails from flow and nonflow environments

The primary function of the gastropod shell is protection. However, shells that function well in one environment may be maladaptive in another. Upon infection, the snail shell protects internal parasites and it is to the parasite's advantage to optimize, or not interfere with, shell functionality. However, parasites, particularly trematodes, are often pathogenic and it is not clear if parasitism will induce environment‐dependent or ‐independent changes to gastropod shells. We conducted a field study and a complementary laboratory experiment to examine the effects of trematode parasitism on shell characteristics (shape, size, and crush resistance) of Physa acuta snails in flow and nonflow environments using geometric morphometrics and crush assays. Field results indicate wetland (nonflow) snails had large, crush resistant shells with narrow apertures and tall spires. In contrast, stream (flow) snails had small, weak shells with wide apertures and short spires. Parasitism had no apparent effect on the crush resistance of wetland snails but significantly reduced the crush resistance of stream snails. Parasitism had no significant effect on overall shell shape in stream or wetland snails. Similar to the results of our field study, nonflow tank snails had significantly more crush resistant shells than flow tank snails. Additionally, the shapes of flow and nonflow tank snails significantly differed where nonflow tank snails resembled wetland snails and flow tank snails resembled stream snails. For laboratory snails, parasitism reduced crush resistance regardless of flow/nonflow treatment. Our results demonstrate that habitat and/or flow treatment was the primary factor affecting P. acuta shell morphology and that trematode parasitism played a secondary role. J. Morphol. 277:316–325, 2016. © 2015 Wiley Periodicals, Inc.     

First Record of Podonominae Larvae Living Phoretically on the Shells of the Water Snail Chilina dombeyana (Diptera: Chironomidae / Gastropoda: Lymnaeidae)

Larvae of Podonomus albinervis Edwards, 1931 were found phoretic on Gastropoda Chilina dombeyana (Bruigière, 1789) on the shores of Lake Nahuel Huapi, in Bariloche, Argentina. Larvae were attached with mucus and some had developed a tube made of detritus on the spire of the snail shell. Adults and pupae with associated larval exuviae were found, which helped to identify the species. Approximately 10% of the snail individuals examined on the shores of the lake had chironomid larvae on their shells. Laboratory observations showed that the midge larvae leave the snail shell when the snail leaves the water, thus demonstrating the phoretic relationship. The high density of both snails and Chironomidae in the littoral habitats of the lake may explain this phoretic relationship.     

不同壳色福寿螺形态性状与体质量的关系

【背景】福寿螺因其食性杂、抗逆性和繁殖力强以及自然天敌少等不断扩散,侵害农作物,被列为我国首批外来入侵物种。国内外学者一直致力于研究对其的防治与监控。自然界中福寿螺存在2种壳色——黄色和黑色,壳色受遗传因素和环境因素的双重影响。广东省福寿螺多以黑色为主,福寿螺倾向于与不同壳色的螺交配。壳色在一定程度上影响其交配的选择性,但2种壳色的福寿螺繁殖力指标差异不显著。而关于这2种壳色的螺在形态学上的差异鲜有报道。【方法】利用生物统计软件和分析方法进行相关性分析、通径分析及多元回归分析,计算相关系数、通径系数和决定系数,研究2种壳色福寿螺形态性状与体质量的关系。【结果】2种壳色福寿螺的体质量、层高的变异系数较大,且黄色比黑色变异系数大。对黄色福寿螺体质量影响较大的依次为壳高、口宽;对黑色福寿螺体质量影响较大的依次为口宽、层高。【结论与意义】2种壳色福寿螺在形态性状方面差异显著,可以将壳色作为特征标记,为福寿螺的监测与灾害评估提供参考。     

Natural selection for apostasy and crypsis acting on the shell colour polymorphism of a mangrove snail, Littoraria filosa (Sowerby) (Gastropoda: Littorinidae)

Littoraria filosa (Sowerby) is a member of the L. scabra group, found amongst the foliage of mangrove trees in northern Australia. The colour of the shell is polymorphic, showing two discrete ground colours, either yellow or orange-pink, with a variable degree of superimposed brown patterning. At a site on Magnetic Island, northern Queensland, colour frequencies of small snails were similar on different backgrounds. Amongst larger shells yellows were more frequent on Avicennia trees with abundant foliage, and browns on relatively bare trees, suggesting that visual selection for crypsis occurred. There was no evidence of substrate selection by the morphs. Yellow shells were cooler than brown shells, but differences in colour frequencies on sunny and shaded trees, and at different seasons, did not suggest climatic selection. By manipulating the colour frequencies of subpopulations of small snails isolated on individual trees, it was shown that the disappearance of yellow and brown shells was frequency-dependent. This result is consistent with hypotheses of mimicry of background elements by the morphs and of apostatic selection by unknown predators. Only the latter can account for the persistence of the highly conspicuous pink morph at a low frequency.     

Sexual selection and non-random mating for shell colour in a natural population of the marine snailLittorina mariae (Gastropoda: Prosobranchia)

In order to estimate the three independent components of mating behaviour, sexual selection in females, sexual selection in males and mating pattern, we studied the distribution of shell colour morphs among mating pairs and between copulating and non-copulating snails in four subsamples of a natural population ofL. mariae. The colour of the shell, the sex and a qualitative estimate of age was recorded for every snail. We found sexual selection acting against one of the two commonest colours (yellow) among the young females. However, in males none of the eight shell colour morphs was favoured during matings. Male sexual choice or differences in female sexual activity may cause the sexual fitness disadvantage of yellow females. Moreover, individuals of different colour morphs did not mate at random, rather dissasortatively. A behavioural choice among shell colour morphs or a non-random microdistribution of the morphs may cause the departure from random mating in this population.     

Natural selection by avian predators on size and colour of a freshwater snail (Pomacea flagellatd)

We identify two avian predators of the Neotropical apple snail, Pomaceaflagellata, and estimate the strength, direction and form of multivariate natural selection by these predators on size and colour of snail shells. Limpkins are tactile predators and act as agents of disruptive selection on snail size, selecting average-sized snails disproportionately more often than small or large snails (y = 0.39, SE = 0.08). In addition, we were able to identify variation in handling behaviours and snail size selection among individual limpkins. Individual limpkins showed preferences for snails of different sizes and punctured the snail shells opposite the aperture mainly when handling large snails. Snail kites are visual predators and seem to be agents of directional selection against lighter coloured snails (β= 0.66, SE = 0.33). The ecological interaction between the apple snail and its predators provides a powerful system to further explore the role of predation in determining evolutionary changes in snail behaviour, morphology and life history.     

A comparative study of the ultrastructure and mineralogy of calcified land snail eggs (Pulmonata: Stylommatophora)

This study indicates that eggs containing calcium carbonate crystals occur in at least 36 of the 65 known families of the land snails (class Gastropoda: order Stylommatophora). Eggs from 22 of these families were available for examination. The x-ray diffraction data, available for the first time for 21 of these families, shows that these egg shells are all made of calcite only, or of a combination of calcite with smaller amounts of aragonite. All of the snail (body) shells examined were made of aragonite only. This is the first ultrastructural investigation of these egg shells, and it indicates that the eggs exhibit enough structural diversity to allow identification of parental animals to genus, and often to species level solely on the basis of egg shell ultrastructure. All of the calcified eggs may be divided into two groups: (1) partly calcified, with discrete crystals of CaCo₃ dispersed in the jelly layer, and (2) heavily calcified, with a hard, brittle egg shell made of fused crystals of CaCO₃ much like an avian egg. Both types of calcified eggs occur in oviparous as well as in ovoviviparous snails. Because of the wide distribution of calcified eggs in the Stylommatophora, and because of the occurrence of heavily calcified eggs in ancient families such as Partulidae, Endodontidae, and Zonitidae, the calcified egg is viewed as a primitive land snail trait associated with terrestrial adaptation. The function of the calcified egg shell, in addition to mechanical support of egg contents, is to supply the developing embryo with enough calcium to form the embryonic shell by the time of hatching.